Gamete Nuclear Migration in Animals and Plants

Fatema, Umma; Ali, Mohammad Foteh; Hu, Zheng; Clark, Anthony; Kawashima, Tomokazu

doi:10.3389/fpls.2019.00517

Cited by 18 publications

(10 citation statements)

References 126 publications

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“…In both animals and plants, karyogamy occurs via a two-step process: pronuclear migration and nuclear membrane fusion ( Fatema et al, 2019 ). During pronuclear migration, one or both pronuclei migrate to become in close proximity, while during nuclear membrane fusion, the nuclear envelopes of the two pronuclei fuse together to produce a zygotic nucleus with both maternal and paternal genomes.…”

Section: Resultsmentioning

confidence: 99%

Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

Hisanaga

Fujimoto

Cui

et al. 2021

eLife

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KNOX and BELL transcription factors regulate distinct steps of diploid development in plants. In the green alga Chlamydomonas reinhardtii, KNOX and BELL proteins are inherited by gametes of the opposite mating types and heterodimerize in zygotes to activate diploid development. By contrast, in land plants such as Physcomitrium patens and Arabidopsis thaliana, KNOX and BELL proteins function in meristem maintenance and organogenesis during the later stages of diploid development. However, whether the contrasting functions of KNOX and BELL were acquired independently in algae and land plants is currently unknown. Here, we show that in the basal land plant species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to initiate zygotic development by promoting nuclear fusion in a manner strikingly similar to that in C. reinhardtii. Our results indicate that zygote activation is the ancestral role of KNOX/BELL transcription factors, which shifted toward meristem maintenance as land plants evolved.

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Section: Resultsmentioning

confidence: 99%

Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

Hisanaga

Fujimoto

Cui

et al. 2021

eLife

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“…Animals produce very distinct kinds of gametes. Gamete fusion determines initial polarity and triggers the developmental programme in animal eggs [218,219], meaning that in earlier stages of animal evolution it could have served as an early trigger for asymmetric cell division, generation of a rudimentary axis and establishment of cell fates. During development and throughout the animal's life, animal cells are able to proliferate in response to signals from within the organism by controlling entry into the cell cycle.…”

Section: Emergence Of a Conjoined Gene Regulatory Programme Of Fertilization And Multicellular Developmentmentioning

confidence: 99%

The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

et al. 2021

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How animals evolved from a single-celled ancestor, transitioning from a unicellular lifestyle to a coordinated multicellular entity, remains a fascinating question. Key events in this transition involved the emergence of processes related to cell adhesion, cell–cell communication and gene regulation. To understand how these capacities evolved, we need to reconstruct the features of both the last common multicellular ancestor of animals and the last unicellular ancestor of animals. In this review, we summarize recent advances in the characterization of these ancestors, inferred by comparative genomic analyses between the earliest branching animals and those radiating later, and between animals and their closest unicellular relatives. We also provide an updated hypothesis regarding the transition to animal multicellularity, which was likely gradual and involved the use of gene regulatory mechanisms in the emergence of early developmental and morphogenetic plans. Finally, we discuss some new avenues of research that will complement these studies in the coming years.

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“…The Arabidopsis central cell is more than five times larger than the egg cell. This large cell size allows us to visualize F-actin dynamics in detail (4,5), thus providing an excellent platform to understand the dynamics of plant fertilization. ROP8 is specifically expressed in the central cell and promotes the assembly of F-actin at the plasma membrane, maintaining the constant F-actin meshwork movement (5).…”

Section: Significancementioning

confidence: 99%

“…After gamete cell fusion, in most animals, both male and female pronuclei move toward each other within the fertilized egg for gamete nuclear fusion, or karyogamy. Pronuclei movement is regulated by microtubules that assemble the sperm aster from the centrosome (3,4). By contrast, flowering plants have lost the centrosome, and have established actin filament (F-actin)-based sperm nuclear migration systems for successful double fertilization (5)(6)(7).…”

mentioning

confidence: 99%

ARP2/3-independent WAVE/SCAR pathway and class XI myosin control sperm nuclear migration in flowering plants

Ali

Fatema

Peng

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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After eukaryotic fertilization, gamete nuclei migrate to fuse parental genomes in order to initiate development of the next generation. In most animals, microtubules control female and male pronuclear migration in the zygote. Flowering plants, on the other hand, have evolved actin filament (F-actin)-based sperm nuclear migration systems for karyogamy. Flowering plants have also evolved a unique double-fertilization process: two female gametophytic cells, the egg and central cells, are each fertilized by a sperm cell. The molecular and cellular mechanisms of how flowering plants utilize and control F-actin for double-fertilization events are largely unknown. Using confocal microscopy live-cell imaging with a combination of pharmacological and genetic approaches, we identified factors involved in F-actin dynamics and sperm nuclear migration inArabidopsis thaliana(Arabidopsis) andNicotiana tabacum(tobacco). We demonstrate that the F-actin regulator, SCAR2, but not the ARP2/3 protein complex, controls the coordinated active F-actin movement. These results imply that an ARP2/3-independent WAVE/SCAR-signaling pathway regulates F-actin dynamics in female gametophytic cells for fertilization. We also identify that the class XI myosin XI-G controls active F-actin movement in theArabidopsiscentral cell. XI-G is not a simple transporter, moving cargos along F-actin, but can generate forces that control the dynamic movement of F-actin for fertilization. Our results provide insights into the mechanisms that control gamete nuclear migration and reveal regulatory pathways for dynamic F-actin movement in flowering plants.

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Gamete Nuclear Migration in Animals and Plants

Cited by 18 publications

References 126 publications

Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

ARP2/3-independent WAVE/SCAR pathway and class XI myosin control sperm nuclear migration in flowering plants

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